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Dynamics and Mechanisms of Adaptive Evolution in Bacteria

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Dynamics and Mechanisms of Adaptive Evolution in Bacteria To my family List of Papers This thesis is based on the following papers, which are referred to in the text by their Roman numerals. I Pettersson ME, Sun S, Andersson DI, Berg OG. (2009). Evolution of new gene functions: simulation and analysis of the amplification model. Genetica 135(3): 309-324. II Sun S, Berg OG, Roth JR, Andersson DI. (2009). Contribution of gene amplification to evolution of increased antibiotic resistance in Salmonella typhimurium. Genetics 182(4): 1183-1195. III Koskiniemi S, Sun S, Berg OG, Andersson DI. (2012). Selection- driven genome reduction in bacteria. (Submitted) IV Sun S, Ke RQ, Hughes D, Nilsson M, Andersson DI. (2012). High frequencies of genome rearrangements in bacterial chromosomes. (Manuscript). V Sun S, Negrea A, Rhen M, Andersson DI. (2009). Genetic analysis of colistin resistance in Salmonella enterica serovar Typhimurium. Antimicrob Agents Chemother 53(6): 2298-2305. VI Sun S, Zhang W, Mannervik B, Andersson DI. (2012). Evolution of increased ß-lactam resistance in an engineered Metallo-ß-lactamase. (Manuscript). Reprints were made with permission from the respective publishers. Contents Introduction ..................................................................................................... 9 Salmonella enterica .................................................................................... 9 Gene duplication and amplification (GDA) ............................................. 10 Dynamics of gene amplification .......................................................... 10 Mechanisms of formation and loss of GDA ........................................ 11 GDA and adaptive evolution ............................................................... 13 Deletion .................................................................................................... 19 Mechanisms of deletion formation ...................................................... 19 Reductive evolution ............................................................................. 21 Inversion ................................................................................................... 22 Formation of inversions ....................................................................... 23 Constraints on inversions ..................................................................... 24 Antibiotic resistance ................................................................................. 24 Resistance mechanisms ........................................................................ 25 Mutation rates ...................................................................................... 26 Spread of antibiotic resistance through HGT ....................................... 27 Fitness cost and compensatory mutations ............................................ 28 Present investigations .................................................................................... 30 Gene amplification promotes innovation of new genes ........................... 30 Gene amplification facilitates antibiotic resistance .................................. 31 Adaptive genome reduction ...................................................................... 33 Detecting spontaneous genome rearrangements ....................................... 35 Genetic analysis of colistin resistance ...................................................... 37 Evolution of a novel Metallo-ß-lactamase ................................................ 38 Connecting penicillin binding proteins and β-lactamases ........................ 39 Concluding remarks .................................................................................. 40 Future perspectives ........................................................................................ 43 Chinese Abstract (摘要) ................................................................................ 45 Acknowledgements ....................................................................................... 46 References ..................................................................................................... 48 Abbreviations S. typhimurium Salmonella enterica serovar Typhimurium strain LT2 E. coli Escherichia coli P. mirabilis Proteus mirabilis DNA Deoxyribonucleic acid RNA Ribonucleic acid mRNA Messenger RNA tRNA Transfer RNA rRNA Ribosomal RNA LPS Lipopolysaccharide ATP Adenosine triphosphate MRSA Methicillin-resistant Staphylococcus aureus NDM-1 New Delhi metallo-β-lactamase 1 PBP Penicillin binding protein ESC Extended spectrum cephalosporin ESBL Extended spectrum β-lactamase MBL Metallo-β-lactamse GTA Gene transfer agents bp Base pair kb Kilo base pairs Mb Mega base pairs GDA Gene duplication and amplification IAD Innovation-amplification-divergence SGR Spontaneous genome rearrangements MMR Methyl-directed mismatch repair BER Base excision repair NER Nucleotide excision repair HGT Horizontal gene transfer MIC Minimum inhibitory concentration PCR Polymerase chain reaction RCR Rolling circle replication PFGE Pulse field gel electrophoresis LB Luria Bertani broth LA Luria Bertani agar Introduction In 1859 Charles Darwin for the first time proposed the theory of evolution by natural selection in his “On the origin of species” (DARWIN 1859) and this revolutionary scientific idea has ever since formed the foundation for understanding the mechanisms of evolution. As one of the major driving forces of evolution, natural selection occurs when a population of individuals differs in their fitness, in other words, their ability to survive and reproduce, and the fittest individuals will become more common in the population. Random genetic drift is another process that drives evolution, whereby chance events fix individuals in the population independent of their fitness (KIMURA 1983). This thesis is focused on the studies of adaptive evolution. Adaptation is the evolutionary process whereby an organism becomes more fit in a particular environment. Although adaptive evolution often leads to complex genetic traits, the underlying process only requires two players: mutation and selection. Mutation is the ultimate source of genetic variation that natural selection works on; therefore determining the properties of mutations is fundamental to understanding the mechanisms of adaptive evolution. Featured by fast generation times, large population sizes, and the ability to be stored in a frozen non-evolving state, microorganisms have been used with great success in laboratory evolution experiments to unravel the genetic basis of adaptation (CONRAD et al. 2011; PORTNOY et al. 2011). In nature, microorganisms are unique for their ability to adapt rapidly to different environments. One significant example is the development of antibiotic resistance. In this thesis, I have investigated the mechanisms of bacterial adaptation to new environments using adaptive laboratory evolution. Different types of mutations were under investigation with a particular interest in genome rearrangements. The adaptation process was focused on the development of bacterial resistance to antibiotics. Salmonella enterica As one of the main workhorses of bacterial genetics, Salmonella enterica serovar Typhimurium strain LT2, hereafter referred to as S. typhimurium, was used as a model organism throughout this work. S. typhimurium is a rod- shaped gram-negative enterobacterium that in humans causes gastroenteritis with symptoms such as diarrhea and fever (HOHMANN 2001). In mice, S. 9 typhimurium causes a systemic infection that is similar to typhoid fever (MASTROENI and SHEPPARD 2004). All strains used in this work derived from the LT2 strain, which is less virulent due to a defective rpoS gene (SWORDS et al. 1997). With a fully sequenced genome (MCCLELLAND et al. 2001), the S. typhimurium LT2 strain has been extensively studied in microbial genetics and a wide range of tools are available for genetic manipulation. Together with the common features shared by microorganisms such as fast growth and large population size, this makes S. typhimurium one of the most convenient model organisms for experimental evolution studies. Gene duplication and amplification (GDA) Gene amplification has been observed in all three kingdoms of life (DEVONSHIRE and FIELD 1991; DUNHAM et al. 2002; ROMERO and PALACIOS 1997; WONG et al. 2007) and is important both from a fundamental evolutionary perspective as a major source of gene novelty (BERGTHORSSON et al. 2007; OHNO 1970), and in medicine as a significant contributor to phenotypic variability among individuals and many human diseases (ALBERTSON 2006; BECKMANN et al. 2007; CONRAD and ANTONARAKIS 2007). Differing from other types of mutations, GDA is more similar to a regulatory response considering its high prevalence and intrinsic instability. With these two properties, GDA is of significant biological importance in adaptive evolution where it can (i) provide a direct solution to a selective problem, (ii) facilitate further adaptation, and (iii) create new gene functions. Dynamics of gene amplification Much of our knowledge about gene amplification comes from the pioneering studies in Escherichia coli (E. coli), S. typhimurium and Proteus mirabilis (P. mirabilis) (ANDERSON and ROTH 1981; ANDERSON and ROTH 1977; HASHIMOTO and ROWND 1975; HILL et al. 1990; PERLMAN and STICKGOLD 1977; PETERSON and ROWND 1985; PETES and HILL 1988; ROTH et al. 1996). These studies not only demonstrated that GDAs are highly prevalent in eubacteria and can affect any gene in bacterial genomes, but also showed that GDAs
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